Effect of cyclosporin A on immunological response in lungs of guinea pigs infected with Trichinella spiralis

• Autorzy: Dzik J. M. , Zielinski Z. , Golos B. , Jagielska E. , Wranicz M. , Walajtys-Rode E.
• Języki publikacji: EN

Abstrakty

EN

The effects of cyclosporin A (CsA), a potent immunosuppressive drug with anti­parasitic activity, on the innate immunological response in guinea pig lungs during an early period (6th and 14th days) after T. spiralis infection were studied. CsA treat­ment of T. spiralis-infected guinea pigs caused a significant attenuation of immuno- logical response in lungs by decreasing lymphocyte infiltration into pulmonary alveo­lar space, inhibiting alveolar macrophage superoxide anion production and lowering both the production of NO metabolites measured in bronchoalveolar lavage fluid and expression of the iNOS protein in lung homogenates, allowing us to speculate that the T. spiralis-dependent immunological response is dependent on lymphocyte T func­tion. Interestingly, CsA itself had a pro-inflammatory effect, promoting leucocyte ac­cumulation and macrophage superoxide production in guinea pig lungs. This observa­tion may have a relevance to the situation in patients undergoing CsA therapy. Macrophage expression of the iNOS protein, evaluated by immunoblotting was not in­fluenced by treatment of animals with CsA or anti-TGF-antibody, indicating different regulation of the guinea pig and murine enzymes.

Słowa kluczowe

EN

superoxide; Trichinella; trichinellosis; nitric oxide; cyclosporin A; bronchoalveolar lavage; lung; Trichinella spiralis

• Wydawca: -
• Czasopismo: Acta Biochimica Polonica
• Rocznik: 2002
• Tom: 49
• Numer: 1
• Opis fizyczny: p.233-247,fig.

Twórcy

autor

Dzik J. M.

• Polish Academy of Sciences, Warsaw, Poland

autor

Zielinski Z.

autor

Golos B.

autor

Jagielska E.

autor

Wranicz M.

autor

Walajtys-Rode E.

Bibliografia

• Attur, M.G., Patel, R., Thakker, G., Vyas, P., Levartovsky, D., Patel, P., Naqvi, S., Raza, R., Patel, K., Abramson, D., Bruno, G., Abramson, S.B. & Amin, A.R. (2000) Differential anti-inflammatory effects of immunosuppressive drugs: Cyclosporin, rapamycin and FK-506 on inducible nitric oxide synthase, nitric oxide, cyclooxygenase-2 and PGE2 production. Inflamm. Res. 49, 20-26.
• Bell, R.G. (1998) The generation and expression of immunity to Trichinella spiralis in laboratory rodents Adv. Parasitol. 41, 149-217.
• Bian, K.A., Harari, Y., Zhong, M., Lai, M., Castro, G., Weibrodt, N. & Murad, F. (2001) Down-regulation of inducible nitric oxide synthase (NOS-2) during parasite-induced gut inflammation: A path to identify a selective NOS-2 inhibitor. Mol. Pharmacol. 59, 939-947.
• Bolas-Fernandez, F., Grencis, R.K. & Wakelin, D. (1988) Cyclosporin A and Trichinella spiralis: Anthelminthic effects in immunosuppressed mice. Parasite. Immunol. 10, 111-116.
• Bruschi, F., Solfanelli, S. & Binaghi, R.A. (1992) Trichinella spiralis: Modifications of the cuticle of the newborn larvae during passage through the lung. Exp. Parasitol. 75, 1-9.
• Bunjes, D., Hardt, C., Rollinghoff, M. & Wagner, H. (1981) Cyclosporin A mediates immunosuppression of primary cytotoxic T cell responses by impairing the release of interleukin 1 and interleukin 2. Eur. J. Immunol. 11, 657-661.
• Burkart, V., Imai, Y., Kallmann, B. & Kolb, H. (1992) Cyclosporin A protects pancreatic islet cells from nitric oxide dependent macrophage cytotoxicity. FEBS Lett. 313, 56-58.
• Calo, L., Semplicini, A., Davis, P.A., Bonvicini, P., Cantaro, S., Rigotti, P., D'Angelo, A., Livi, U. & Antonello, A. (2000) Cyclosporin-induced endothelial dysfunction and hypertension: Are nitric oxide system abnormality and oxidative stress involved? Transpl. Int. 13(Suppl. 1), S413-S418.
• Ceyhan, B.B., Sungur, M., Celikel, C.A. & Celikel, T. (1998) Effect of inhaled cyclosporin on the rat airway: Histologic and bronchoalveolar lavage assessment. Respiration 65, 71-78.
• Chapman, I. & Mazzoni, L. (1994) Mechanisms of inhibition by cyclosporin A on pulmonary leukocyte accumulation. Trends Parasitol. Sci. 124, 43-48.
• Chappel, L. & Wastling, J.M. (1992) Cyclosporin A: Antiparasite drug, modulator of the host- parasite relationship and immunosuppressant. Parasitology 105 (Suppl.), S25-S40.
• Chiara, M.D., Bedoya, F. & Sobrino, F. (1989). Cyclosporin A inhibits phorbol ester-induced activation of superoxide production in resident mouse peritoneal macrophages. Biochem. J. 264, 21-26.
• Colombani, P.M. & Hess, A.D. (1987) T-Lymphocyte inhibition by cyclosporine. Potential mechanism of action. Biochem. Pharmacol. 36, 3789-3793.
• Conde, M., Andrade, J., Bedoya, F.J., Santa Maria, C. & Sobrino, F. (1995) Inhibitory effect of cyclosporin A and FK506 on nitric oxide production by cultured macrophages. Evidence of a direct effect on nitric oxide synthase activity. Immunology 84, 476-481.
• Dabrowska, M., Zielinski, Z., Wranicz, M., Michalski, R., Pawelczak, K. & Rode, W. (1996) Trichinella spiralis thymidylate synthase: Developmental pattern, isolation, molecular properties and inhibition by substrate and cofactor analogues. Biochem. Biophys. Res. Commun. 228, 440-445.
• De Caterina, R., Tanaka, H., Nakagawa, T., Hauptman, P.J. & Libby, P. (1995) The direct effect of injectable cyclosporine and its vehicle, cremophor, on endothelial vascular cell adhesion molecule-1 expression. Ricinoleic acid inhibits coronary artery endothelial activation. Transplantation 60, 270-275.
• Denis, M., Cormier, Y. & Laviolette, M. (1992) Murine hypersensitivity pneumonitis: A study of cellular infiltrates and cytokine production and its modulation by cyclosporin A. Am. J. Respir. Cell Mol. Biol. 6, 68-74.
• Despommier, D.D. (1993) Trichinella spiralis and the concept of niche. J. Parasitol. 79, 472- 482.
• Dick, A.D., Kreutzer, B., Laliotou, B. & Forrester, J.V. (1997) Phenotypic analysis of retinal leukocyte infiltration during combined cyclosporin A and nasal antigen administration of retinal antigens: Delay and inhibition of macrophage and granulocyte infiltration. Ocul. Immunol. Inflamm. 5, 129-140.
• Dzik, J.M., Golos, B., Kapala, A., Wranicz, M. & Walajtys-Rode, E. (2000) Guinea pig lungs response to Trichinella spiralis infection. Acta Parasitol. 45, 192.
• Egwang, T.G., Gauldie, J., & Befus, D. (1984) Broncho-alveolar leucocyte response during primary and secondary Nippostrongylus brasiliensis infection in the rat. Parasite Immunol. 6, 191-201.
• Elwood, W., Lotwall, J.O., Barnes, P.J. & Chung K.F. (1992) Effect of dexamethasone and cyclosporin A on allergen- induced airway hyperresponsiveness and inflammatory cell responses in sensitized Brown-Norway rats. Am. Rev. Respir. Dis. 145, 1289-1294.
• Forman, H.J., Zhou, H., Gozal, E. & Torres, M. (1998) Modulation of the alveolar macrophage superoxide production by protein phosphorylation. Environ. Health Perspect. 106, (Suppl. 5) 1185-1190.
• Gilliam, M.B., Sherman, M.P., Griscavage, J.M.Z. & Ignarro, L.J. (1993) A spectrophotometric assay for nitrate using NADPH oxidation by Aspergillus nitrate reductase. Anal. Biochem. 212, 359-365.
• Green, L.C., Wagner, D.A., Glogowski, J., Skipper, P.I., Wishnok, J.S. & Tannenbaum, S.R. (1982) Analysis of nitrate, nitrite and [15N]nitrate in biological fluids Anal. Biochem. 126, 131-138.
• Hattori, Y. & Nakanishi, N. (1995) Effect of cyclosporin A and FK506 on nitric oxide and tetrahydrobiopterin synthesis in bacterial lipopolysaccharide-treated J774 macrophages. Cell. Immunol. 165, 7-11.
• Issekutz, T.B. (1989) Effects of anti-inflammatory agents on lymphocyte migration stimulated by the interferons, tumor necrosis factor and cutaneous inflammation. Int. J. Immunopharmacol. 11, 725-732.
• Iyengar, R., Stuehr, D.J. & Marietta, M.A. (1987) Macrophage synthesis of nitrite, nitrate, and N-nitrosoamines: Precursors and role of the respiratory burst. Proc. Natl. Acad. Sci. U.S.A. 84, 6369-6373.
• James, S.L. (1995) Role of nitric oxide in parasitic infections. Microbiol. Rev. 59, 533-547.
• Jesch, N.K., Dorger, M., Enders, G., Rieder, G., Vogelmeier, C.F., Messmer, K. & Krombach, F. (1997) Expression of inducible nitric oxide synthase and formation of nitric oxide by alveolar macrophages: An interspecies comparison. Environ. Health Perspect. 105 (Suppl. 5), 1297-1300.
• Kahan, B.D. (1994) Role of cyclosporine: present and future. Transplant. Proc. 26, 3082-3087.
• Kunz, D., Walker, G., Eberhardt, W., Nitsch, D. & Pfeilschifter, J. (1995) Interleukin 1-beta-induced expression of nitric oxide synthase in rat renal mesangial cells is suppressed by cyclosporin A. Biochem. Biophys. Res. Commun. 216, 438-446.
• Lagente, V., Carre, C., Kyriacopoulos, F., Boichot, E., Mencia-Huerta, J.M. & Braquet, P. (1994) Inhibitory effect of cyclosporin A on eosinophil infiltration in the guinea-pig lung induced by antigen, platelet-activating factor and leukotriene B4. Eur. Respir. J. 7, 921-926.
• Lindor, L.J., Wassom, D.L. & Gleich, G.J. (1983) Effects of trichinellosis on levels of eosinophils, eosinophil major basic protein, creatine kinase and basophils in the guinea pig. Parasite Immunol. 5, 13-24.
• Liu, J., Farmer, J.D., Lane, W.S., Friedman, J., Weissman, I. & Schreiber, S.L. (1991) Calcineurin is a common target of cyclophilin, cyclosporin A and FKBK-FK506 complexes. Cell66, 807-815.
• Losa Garcia, J.E., Mateos Rodriguez, F., Jimenez Lopez, A., Garcia Salgado, M.J., Martin de Cabo, M.R., Perez Losada, J. & Perez Arellano, J.L. (1998) Effect of cyclosporin A on inflammatory cytokine production by human alveolar macrophages. Respir. Med. 92, 722-728.
• Lu, D.J., Takai, A., Leto, T.L. & Grinstein, S. (1992) Modulation of neutrophil activation by okadaic acid, a protein phosphatase inhibitor. Am. J. Physiol. 262, (Part 1) C39-C49.
• Miller, H.R.P. (1984) The protective mucosal response against gastrointestinal nematodes in ruminants and laboratory animals. Vet. Immunol. Immunopathol. 6, 167-259.
• Miller, R.A. & Britigan, B.E. (1997) Role of oxidants in microbial pathophysiology. Clin. Microbiol. Rev. 10, 1-18.
• Morel, F., Doussiere, J. & Vignais, P.V. (1991) The superoxide-generating oxidase of phagocytic cells. Physiological, molecular and pathological aspects. Eur. J. Biochem. 201, 523-546.
• Morris, S.M., Jr. & Billiar, T.R. (1994) New insights into the regulation of inducible nitric oxide synthesis. Am. J. Physiol. 266 (Part 2), E829-E839.
• Muramo, T., Nakaki, T., Hishikawa, K., Suzuki, H. Kato, R. & Saruta, T. (1995) Cyclosporin A inhibits nitric oxide synthase induction in vascular smooth muscle cells. Hypertension 25, 764-768.
• Nathan, C. & Xie, Q.W. (1994) Regulation of biosynthesis of nitric oxide. J. Biol. Chem. 269, 13725-13728.
• Navarro-Antolin, J., Rey-Campos, J. & Lamas, S. (2000) Transcriptional induction of endothelial nitric oxide gene by cyclosporin A. A role for activator protein-1. J. Biol. Chem. 275, 3075-3080.
• Nijkamp, F.P., van der Linde, H.J., Folkerts, G. (1993) Nitric oxide synthesis inhibitors induce airway hyperresponsiveness in guinea pig in vivo and in vitro. Role of the epithelium. Am. Rev. Respir. Dis. 148, 727-734.
• Norris, A.A., Jackson, D.M. & Eady, R.P. (1992) Protective effects of cyclophosphamide, cyclosporin A and FK506 against antigen-induced lung eosinophilia in guinea-pigs. Clin. Exp. Immunol. 89, 347-350.
• Oswald, I.P., Wynn, T.A., Sher, A. & James, S.L. (1994) NO as an effector molecule of parasite killing: Modulation of its synthesis by cytokines. Comp. Biochem. Physiol. Pharmacol. Toxicol. Endocrinol. 108, 11-18.
• Prud' homme, G.P. & Vanier, L.E. (1993) Cyclosporine, tolerance, and autoimmunity. Clin. Immunol. Immunopathol. 66, 185-192.
• Rajagopalan-Levassieur, P., Lecointe, D., Bertrand, G., Fay, M. & Gougerot, M.A. (1996) Differential nitric oxide (NO) production by macrophages from mice and guinea pigs infected with virulent and avirulent Legionella pneumophilia serogrup 1. Clin. Exp. Immunol. 104, 48-53.
• Rochelle, L.G., Fischer, B.M. & Adler, K.B. (1998) Concurrent production of reactive oxygen and nitrogen species by airway epithelial cells in vitro. Free Radicals Biol. Med. 24, 863-868.
• Salter, M., Knowles, R.G. & Moncada, S. (1991) Widespread tissue distribution, species and changes in activity of Ca2+- dependent and Ca2+ -independent nitric oxide synthases. FEBS Lett. 291, 145-149.
• Shirato, M., Sakamoto, T., Uchida, Y., Nomura, A., Ishii, Y., Iijima, H., Goto, Y. & Hagesawa, S. (1998) Molecular cloning and characterization of Ca2+-dependent inducible nitric oxide synthase from guinea-pig lung. Biochem. J. 333, 795-799.
• Siegel, S. (1956) Nonparametric Statistics for the Behavioral Sciences. Mc Graw-Hill Kogakusha Ltd., Tokyo.
• Spector, T. (1978) Refinement of the Coomassie Blue method of protein quantitation. Anal. Biochem. 86, 142-146.
• Suleymanlar, G., Suleymanlar, I., Shapiro, J.I. & Chan, L. (1994) Possible role of lipid peroxidation in cyclosporine nephrotoxicity in rats. Transpl. Proc. 26, 2888-2889.
• Svensson, U., Holst, E. & Sundler, R. (1995) Cyclosporin-sensitive expression of cytokine mRNA in mouse macrophages responding to bacteria. Mol. Immunol. 32, 157-165.
• Taskinen, H.S. & Roytta, M. (2000) Cyclosporin A affects axons and macrophage during Wallerian degeneration. J. Neurotrauma. 17, 431-440.
• Teixeira, M.M., Williams, T.J. & Hellewell, P.G. (1996) Effects of dexamethasone and cyclosporin A on the accumulation of eosinophils in acute cutaneous inflammation in the guinea pigs. Br. J. Pharmacol. 118, 317-324.
• Thomson, A.W. (1992) The effects of cyclosporin A on non-T cell components of the immune system. J. Autoimmun. 5 (Suppl A), 167-176.
• Vodovotz, Y. (1997) Control of nitric oxide production by transforming growth factor-beta1: Mechanistic insight and potential relevance to human disease. Nitric Oxide. 1, 3-17.
• Vodovotz, Y., Letterio, J.J., Geiser, A.G., Chesler, L., Roberts, A.B. & Sparrow, J. (1996) Control of nitric oxide production by endogenous TGF-beta1 and systemic nitric oxide in retinal pigment epithelial cells and peritoneal macrophages. J. Leukoc. Biol. 60, 261-270.
• Wang, C.H. & Bell, RG. (1986) Trichinella spiralis: Vascular recirculation and organ retention of newborn larvae in rats. Exp. Parasitol. 62, 430-441.
• Wang, J.M., Denis, M., Fournier, M. & Laviolette, M. (1993) Cyclosporin A increases the pulmonary eosinophilia induced by inhaled Aspergillus antigen in mice. Clin. Exp. Immunol. 93, 323-330.
• Weatherly, N.F. (1983) Anatomical pathology; in Trichinella and Trichinellosis (Campbell, W.C., ed.) pp. 173-208, Plenum Press, New York, NY.
• Weinberg, J.B., Misukonis, M.A., Shami, P.J., Mason, S.N., Sauls, D.L., Dittman, W.A., Wood, E,R., Smith, G,K., McDonald, B., Bachus, K.E., Haney, A.F. & Granger, D.L. (1995) Human mononuclear phagocyte inducible nitric oxide synthase (iNOS): Analysis of iNOS mRNA, iNOS protein, biopterin, and nitric oxide production by blood monocytes and peritoneal macrophages. Blood 86, 1184-1195.
• Wolf, A., Trendelenburg, C.-F., Diez-Fernandez, C., Prieto, P. & Cordier, A. (1994) Role of glutathione in cyclosporine A in vitro hepatotoxicity. Transpl. Proc. 26, 2912-2914.
• Xia, H. & Bredt, S. (1998) Cloned and expressed nitric oxide synthase proteins. Methods Enzymol. 268(Part A), 427-436.
• Yamashita, T., Someya, A. & Hara, E. (1985) Response of superoxide anion production by guinea-pig eosinophils to various soluble stimuli: Comparison to neutrophils. Arch. Biochem. Biophys. 241, 447-452.
• Zhang, X. & McMurray, D.N. (1998) Suppression of lymphoproliferation by alveolar macrophages in the guinea pig. Tuber. Lung Dis. 79, 119-126.